Skip to main content

Advertisement

Log in

Review of the diversity, traits, and ecology of zooxanthellate jellyfishes

  • Review, Concept, and Synthesis
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Many marine organisms form photosymbioses with zooxanthellae, but some, such as the medusozoans, are less well known. Here, we summarize the current knowledge on the diversity of zooxanthellate jellyfishes, to identify key traits of the holobionts, and to examine the impact of these traits on their ecology. Photosymbiosis with zooxanthellae originated at least seven times independently in Medusozoa; of these, five involve taxa with medusae. While most zooxanthellate jellyfishes are found in clades containing mainly non-zooxanthellate members, the sub-order Kolpophorae (Scyphozoa: Rhizostomeae) is comprised—bar a few intriguing exceptions—of only zooxanthellate jellyfishes. We estimate that 20–25% of Scyphozoa species are zooxanthellate (facultative symbiotic species included). Zooxanthellae play a key role in scyphozoan life-cycle and nutrition although substantial variation is observed during ontogeny, or at the intra- and inter-specific levels. Nonetheless, three key traits of zooxanthellate jellyfishes can be identified: (1) zooxanthellate medusae, as holobionts, are generally mixotrophic, deriving their nutrition both from predation and photosynthesis; (2) zooxanthellate polyps, although capable of hosting zooxanthellae rarely depend on them; and (3) zooxanthellae play a key role in the life-cycle of the jellyfish by allowing or facilitating strobilation. We discuss how these traits might help to explain some aspects of the ecology of zooxanthellate jellyfishes—notably their generally low ability to outbreak, and their reaction to temperature stress or to eutrophication—and how they could in turn impact marine ecosystem functioning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arai MN (1997) A functional biology of Scyphozoa. Chapman & Hall, London

    Google Scholar 

  • Arai MN (2001) Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451:69–87

    Article  Google Scholar 

  • Astorga D, Ruiz J, Prieto L (2012) Ecological aspects of early life stages of Cotylorhiza tuberculata (Scyphozoa: Rhizostomae) affecting its pelagic population success. Hydrobiologia 690:141–155

    Article  Google Scholar 

  • Banaszak AT, Iglesias-Prieto R, Trench RK (1993) Scrippsiella velellae sp. nov. (Peridiniales) and Gloeodinium viscum sp. nov. (Phytodiniales), Dinoflagellate symbionts of two hydrozoans (Cnidaria). J Phycol 29:517–528

    Article  Google Scholar 

  • Bayha KM, Graham WM (2014) Nonindigenous marine jellyfish: invasiveness, invasibility, and impacts. In: Pitt K, Lucas C (eds) Jellyfish blooms. Springer, Dordrecht, pp 45–77

    Chapter  Google Scholar 

  • Bayha KM, Dawson MN, Collins AG, Barbeitos MS, Haddock SHD (2010) Evolutionary relationships among scyphozoan jellyfish families based on complete taxon sampling and phylogenetic analyses of 18S and 28S ribosomal DNA. Integr Comp Biol 50:436–455

    Article  CAS  PubMed  Google Scholar 

  • Bezio N, Costello JH, Perry E, Colin SP (2018) Effect of capture surface morphology on feeding success of scyphomedusae: a comparative study. Mar Ecol Prog Ser 596:83–93

    Article  Google Scholar 

  • Bieri R (1977) The ecological significance of seasonal occurrence and growth rate of Velella (Hydrozoa). Publ Seto Mar Biol Lab 24:63–76

    Article  Google Scholar 

  • Billett DSM, Bett BJ, Jacobs CL, Rouse IP, Wigham BD (2006) Mass deposition of jellyfish in the deep Arabian Sea. Limnol Oceanogr 51:2077–2083

    Article  Google Scholar 

  • Blanquet RS, Phelan MA (1987) An unusual blue mesogleal protein from the mangrove jellyfish Cassiopea xamachana. Mar Biol 94:423–430

    Article  CAS  Google Scholar 

  • Blanquet RS, Riordan GP (1981) An ultrastructural study of the subumbrellar musculature and desmesomal complexes of Cassiopea xamachana (Cnidaria: Scyphozoa). Trans Am Microsc Soc 100:109–119

    Article  Google Scholar 

  • Boero F, Brotz L, Gibbons MJ, Piraino S, Zampardi S (2016) Impacts and effects of ocean warming on jellyfish. In: Laffoley D, Baxter JM (eds) Explaining ocean warming: causes, scale, effects and consequences. IUCN, Gland, pp 213–237

    Google Scholar 

  • Bolton TF, Graham WM (2004) Morphological variation among populations of an invasive jellyfish. Mar Ecol Prog Ser 278:125–139

    Article  Google Scholar 

  • Bouillon J (1984) Hydroméduses de la mer de Bismarck (Papouasie Nouvelle-Guinée. Partie IV: Leptomedusae (Hydrozoa-Cnidaria). Indo-Malayan Zool 1:25–112

    Google Scholar 

  • Bouillon J, Seghers G, Boero F (1988) Notes additionnelles sur les méduses de Papouasie Nouvelle-Guinée (Hydrozoa, Cnidaria) III. Indo-Malayan Zool 5:225–253

    Google Scholar 

  • Bouillon J, Gravili C, Pagès F, Gili J-M, Boero F (2006) An introduction to Hydrozoa. Publications Scientifiques du Muséum, Paris

    Google Scholar 

  • Brinckmann-Voss A, Arai MN (1998) Further notes on Leptolida (Hydrozoa: Cnidaria) from Canadian Pacific waters. Zool Verh 323:37–68

    Google Scholar 

  • Brooks WK (1903) On a new genus of hydroid jelly-fishes. Proc Am Phil Soc 42:11–14

    Google Scholar 

  • Calder DR (1991) Shallow-water hydroids of Bermuda: the Thecatae, exclusive of Plumularioidea. R Ont Mus Publ Life Sci 154:1–140

    Google Scholar 

  • Carrette T, Straehler-Pohl I, Seymour J (2014) Early life history of Alatina cf. moseri populations from Australia and Hawaii with implications for taxonomy (Cubozoa: Carybdeida, Alatinidae). PLoS One 9:e84377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cates N (1975) Productivity and organic consumption in Cassiopea and Condylactus. J Exp Mar Biol Ecol 18:55–59

    Article  Google Scholar 

  • Cates N, McLaughlin JJA (1976) Differences of ammonia metabolism in symbiotic and aposymbiotic Condylactus and Cassiopea spp. J Exp Mar Biol Ecol 21:1–5

    Article  CAS  Google Scholar 

  • Cimino MA, Patris S, Ucharm G, Bell LJ, Terrill E (2018) Jellyfish distribution and abundance in relation to the physical habitat of Jellyfish Lake, Palau. J Trop Ecol 34:17–31

    Article  Google Scholar 

  • Colley NJ, Trench RK (1985) Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate. Cell Tissue Res 239:93–103

    Article  CAS  PubMed  Google Scholar 

  • Condon RH, Steinberg DK, del Giorgio PA, Bouvier TC, Bronk DA, Graham WM, Ducklow HW (2011) Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc Nat Acad Sci USA 108:10225–10230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Condon RH, Duarte CM, Pitt KA, Robinson KL, Lucas CH, Sutherland KR, Mianzan HW, Bogeberg M, Purcell JE, Decker MB, Uye S-I, Madin LP, Brodeur RD, Haddock SHD, Malej A, Parry GD, Eriksen E, Quiñones J, Acha M, Harvey M, Arthur JM, Graham WM (2013) Recurrent jellyfish blooms are a consequence of global oscillations. Proc Nat Acad Sci USA 110:1000–1005

    Article  CAS  PubMed  Google Scholar 

  • Costello JH, Kremer PM (1989) Circadian rhythmicity in the location of zooxanthellae of the scyphomedusa Linuche unguiculata. Mar Ecol Prog Ser 57:279–286

    Article  Google Scholar 

  • Cruz-Rivera E, El-Regal MA (2015) A bloom of an edible scyphozoan jellyfish in the Red Sea. Mar Biodivers 46:515–519

    Article  Google Scholar 

  • Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293

    Article  Google Scholar 

  • da Silveira FL, Morandini AC (1997) Nausithoe aurea n. sp. (Scyphozoa, Coronatae: Nausithoidae), a species with two pathways of reproduction after strobilation: sexual and asexual. Contrib Zool 66:235–246

    Google Scholar 

  • da Silveira FL, Morandini AC (1998) Asexual reproduction in Linuche unguiculata (Swartz, 1788) (Scyphzoa: Coronatae) by planuloid formation through strobilation and segmentation. Proc Biol Soc Washington 111:781–794

    Google Scholar 

  • Daly M, Brugler MR, Cartwright P, Collins AG, Dawson MN, Fautin DG, France SC, McFadden CS, Opresko DM, Rodriguez E, Romano SL, Stake JL (2007) The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182

    Article  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of Cnidarian-Dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson MN (2005) Morphological variation and systematics in the Scyphozoa: Mastigias (Rhizostomeae, Mastigiidae)—a golden unstandard? Hydrobiologia 537:185–206

    Article  Google Scholar 

  • Dawson MN, Hamner WM (2003) Geographic variation and behavioral evolution in marine plankton: the case of Mastigias (Scyphozoa, Rhizostomeae). Mar Biol 143:1161–1174

    Article  Google Scholar 

  • Dawson MN, Hamner WM (2009) A character-based analysis of the evolution of jellyfish blooms: adaptation and exaptation. Hydrobiologia 616:193–215

    Article  Google Scholar 

  • Dawson MN, Martin LE (2001) Geographic variations and ecological adaptation in Aurelia (Scyphozoa, Semeostomeae): some implications from molecular phylogenetics. Hydrobiologia 451:259–273

    Article  Google Scholar 

  • Dawson MN, Martin LE, Penland LK (2001) Jellyfish swarms, tourists, and the Christ-child. Hydrobiologia 451:131–144

    Article  Google Scholar 

  • de Souza LM, Iacomini M, Gorin PAJ, Sari RS, Haddad MA, Sassaki GL (2007) Glyco- and sphingophoslipids from the medusa Phyllorhiza punctata: NMR and ESI-MS/MS fingerprints. Chem Phys Lipids 145:85–96

    Article  PubMed  CAS  Google Scholar 

  • Drew EA (1972) The biology and physiology of alga-invertebrate symbioses. I. Carbon fixation in Cassiopea sp. at Aldabra Atoll. J Exp Mar Biol Ecol 9:65–69

    Article  CAS  Google Scholar 

  • Duarte CM, Pitt KA, Lucas CH, Purcell JE, Uye S-I, Robinson K, Brotz L, Decker MB, Sutherland KR, Malej A, Madin L, Mianzan H, Gili J-M, Fuentes V, Atienza D, Pagés F, Breitburg D, Malek J, Graham WM, Condon RH (2012) Is global ocean sprawl a cause of jellyfish blooms? Front Ecol Environ 11:91–97

    Article  Google Scholar 

  • Estes AM, Kempf SC, Henry RP (2003) Localization and quantification of carbonic anhydrase activity in the symbiotic scyphozoan Cassiopea xamachana. Biol Bull 204:278–289

    Article  CAS  PubMed  Google Scholar 

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  PubMed  Google Scholar 

  • Ferrier-Pagès C, Leal MC (2018) Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses. Ecol Evol 9:723–740

    PubMed  PubMed Central  Google Scholar 

  • Fitt WK (1984) The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and molluscs with zooxanthellae. Mar Biol 81:9–17

    Article  Google Scholar 

  • Fitt WK, Cook CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Mar Biol 139:507–517

    Article  Google Scholar 

  • Fitt WK, Costley K (1998) The role of temperature in survival of the polyp stage of the tropical rhizostome jellyfish Cassiopea xamachana. J Exp Mar Biol Ecol 222:79–91

    Article  Google Scholar 

  • Fleck J, Fitt WK (1999) Degrading mangrove leaves of Rhizophora mangle Linne provide a natural cue for settlement and metamorphosis of the upside down jellyfish Cassiopea xamachana Bigelow. J Exp Mar Biol Ecol 234:83–94

    Article  Google Scholar 

  • Freeman CJ, Stoner EW, Easson CG, Matterson KO, Baker DM (2016) Symbiont carbon and nitrogen assimilation in the Cassiopea-Symbiodinium mutualism. Mar Ecol Prog Ser 544:281–286

    Article  CAS  Google Scholar 

  • Freeman CJ, Stoner EW, Easson CG, Matterson KO, Baker DM (2017) Variation in δ13C and δ15N values suggests a coupling of host and symbiont metabolism in the Symbiodinium-Cassiopea mutualism. Mar Ecol Prog Ser 571:245–251

    Article  CAS  Google Scholar 

  • Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J Protozool 9:45–52

    Article  Google Scholar 

  • Fuentes V, Straehler-Pohl I, Atienza D, Franco I, Tilves U, Gentile M, Acevedo M, Oleriaga A, Gili J-M (2011) Life cycle of the jellyfish Rhizostoma pulmo (Scyphozoa: Rhizostomeae) and its distribution, seasonality and inter-annual variability along the Catalan coast and the Mar Menor (Spain, NW Mediterranean). Mar Biol 158:2247–2266

    Article  Google Scholar 

  • Furla P, Richier S, Allemand D (2011) Physiological adaptation to symbiosis in cnidarians. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 187–195

    Chapter  Google Scholar 

  • Galea HR, Ferry R (2015) Notes on some hydroids (Cnidaria) from Martinique, with descriptions of five new species. Rev Suisse Zool 122:213–246

    Google Scholar 

  • García JR (1990) Population dynamics and production of Phyllorhiza punctata (Cnidaria: Scyphozoa) in Laguna Joyuda, Puerto Rico. Mar Ecol Prog Ser 64:243–251

    Article  Google Scholar 

  • García JR, Durbin E (1993) Zooplanktivorous predation by large scyphomedusae Phyllorhiza punctata (Cnidaria: Scyphozoa) in Laguna Joyuda. J Exp Mar Biol Ecol 173:71–93

    Article  Google Scholar 

  • Gershwin L, Davie PJF (2013) A remarkable new jellyfish (Cnidaria: Scyphozoa) from coastal Australia, representing a new suborder within the Rhizostomeae. Mem Queensl Mus 56:625–630

    Google Scholar 

  • Gómez Daglio L, Dawson MN (2017) Species richness of jellyfishes (Scyphozoa: Discomedusae) in the Tropical Eastern Pacific: missed taxa, molecules, and morphology match in a biodiversity hotspot. Invertebr Syst 31:635–663

    Article  Google Scholar 

  • Graham WM, Martin DL, Felder DL, Asper VL, Perry HM (2003) Ecological and economic implications of a tropical jellyfish invader in the Gulf of Mexico. Biol Invasions 5:53–69

    Article  Google Scholar 

  • Gueroun SKM, Kéfi-Daly Yahia O, Deidun A, Fuentes V, Piraino S, Daly Yahia MN (2014) First record and potential trophic impact of Phyllorhiza punctata (Cnidaria: Scyphozoa) along the north Tunisian coast (South Western Mediterranean Sea). Ital J Zool 8:95–100

    Google Scholar 

  • Haddad MA, Nogueira Júnior M (2006) Reappearance and seasonality of Phyllorhiza punctata von Lendenfeld (Cnidaria, Scyphozoa, Rhizostomeae) medusae in southern Brazil. Rev Bras Zool 23:824–831

    Article  Google Scholar 

  • Hamner WM, Hauri IR (1981) Long-distance horizontal migrations of zooplankton (Scyphomedusae: Mastigias). Limnol Oceanogr 26:414–423

    Article  Google Scholar 

  • Hamner WM, Gilmer RW, Hamner PP (1982) The physical, chemical, and biological characteristics of a stratified, saline, sulfide lake in Palau. Limnol Oceanogr 27:896–909

    Article  CAS  Google Scholar 

  • Hartmann AC, Marhaver KL, Klueter A, Lovci MT, Closek CJ, Diaz E, Chamberland VF, Archer FI, Deheyn DD, Vermeij MJA, Medina M (2019) Acquisition of obligate symbionts during the larval stage is not beneficial for a coral host. Mol Ecol 28:141–155

    Article  PubMed  Google Scholar 

  • Hays GC, Doyle TK, Houghton JDR (2018) A paradigm shift in the trophic importance of jellyfish? Trends Ecol Evol 33:874–884

    Article  PubMed  Google Scholar 

  • Heins A, Glatzel T, Holst S (2015) Revised descriptions of the nematocysts and the asexual reproduction modes of the scyphozoan jellyfish Cassiopea andromeda (Forskål, 1775). Zoomorphology 134:351–366

    Article  Google Scholar 

  • Helm RR (2018) Evolution and development of scyphozoan jellyfish. Biol Rev 93:1228–1250

    Article  PubMed  Google Scholar 

  • Hofmann DK, Kremer BP (1981) Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): Significance of endosymbiotic Dinoflagellates. Mar Biol 65:25–33

    Article  CAS  Google Scholar 

  • Hofmann DK, Neumann R, Henne K (1978) Strobilation budding and initiation of scyphistome morphogenesis in the Rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Mar Biol 47:161–176

    Article  Google Scholar 

  • Hofmann DK, Fitt WK, Fleck J (1996) Checkpoints in the life-cycle of Cassiopea spp.: control of metagenesis and metamorphosis in a tropical jellyfish. Int J Dev Biol 40:331–338

    CAS  PubMed  Google Scholar 

  • Holland BS, Dawson MN, Crow GL, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128

    Article  Google Scholar 

  • Jantzen C, Wild C, Rasheed M, El-Zibdah M, Richter C (2010) Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef. Mar Ecol Prog Ser 411:117–125

    Article  Google Scholar 

  • Kayal E, Bentlage B, Cartwright P, Yanagihara AA, Lindsay DJ, Hopcroft RR, Collins AG (2015) Phylogenetic analysis of higher-level relationships within Hydroidolina (Cnidaria: Hydrozoa) using mitochondrial genome data and insight into their mitochondrial transcription. PeerJ 3:e1403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kayal E, Bentlage B, Pankey MS, Ohdera AH, Medina M, Plachetzki DC, Collins AG, Ryan JF (2018) Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits. BMC Evol Biol 18:68

    Article  PubMed Central  CAS  Google Scholar 

  • Kikinger R (1992) Cotylorhiza tuberculata (Cnidaria: Scyphozoa—Life history of a stationary population. Mar Ecol 13:333–362

    Article  Google Scholar 

  • Klein SG, Pitt KA, Nitschke MR, Goyen S, Welsh DT, Suggett DJ, Carroll AR (2017) Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian. Glob Change Biol 23:3690–3703

    Article  Google Scholar 

  • Klein SG, Pitt KA, Lucas CH, Hung S-H, Schmidt-Roach S, Aranda M, Duarte CM (2019) Night-time temperature reprieves enhances the thermal tolerance of a symbiotic cnidarian. Front Mar Sci 6:453

    Article  Google Scholar 

  • Kramp PL (1961) Synopsis of the medusae of the world. J Mar Biol Assoc UK 40:1–469

    Google Scholar 

  • Kremer P (2005) Ingestion and elemental budgets for Linuche unguiculata, a scyphomedusa with zooxanthellae. J Mar Biol Assoc UK 85:613–625

    Article  Google Scholar 

  • Kremer P, Costello J, Kremer J, Canino M (1990) Significance of photosynthetic endosymbionts to the carbon budget of the schyphomedusa Linuche unguiculata. Limnol Oceanogr 35:609–624

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    Article  CAS  PubMed  Google Scholar 

  • Lampert KP (2016) Cassiopea and its zooxanthellae. In: Goffredo S, Dubinsky Z (eds) The cnidaria, past, present and future. Springer, Cham, pp 415–423

    Chapter  Google Scholar 

  • Lampert KP, Bürger P, Striewski S, Tollrian R (2012) Lack of association between color morphs of the jellyfish Cassiopea andromeda and zooxanthella clade. Mar Ecol 33:364–369

    Article  Google Scholar 

  • Lapointe BE, Brewton RA, Herren LW, Porter JW, Hu C (2019) Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study. Mar Biol 166:108

    Article  CAS  Google Scholar 

  • Larson RJ (1980) The medusae of Velella velella (Linnaeus, 1758) (Hydrozoa, Chondrophorae). J Plankton Res 2:183–186

    Article  Google Scholar 

  • Larson RJ (1992) Riding Langmuir circulations and swimming in circle: a novel form of clustering behavior by the scyphomedusa Linuche unguiculata. Mar Biol 112:229–235

    Article  Google Scholar 

  • Larson RJ (1997) Feeding behaviour of Caribbean scyphomedusae: Cassiopea frondosa (Pallas) and Cassiopea xamachana Bigelow. Stud Nat Hist Caribbean Reg 73:43–54

    Google Scholar 

  • Lesser MP, Stat M, Gates RD (2013) The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32:603–611

    Article  Google Scholar 

  • Lewis JB (1991) The ampullae and medusae of the calcareous hydrozoan Millepora complanata. Hydrobiologia 216(217):165–169

    Article  Google Scholar 

  • Lewis JB (2006) Biology and ecology of the hydrocoral Millepora on coral reefs. Adv Mar Biol 50:1–55

    Article  PubMed  Google Scholar 

  • Lopes AR, Baptista M, Rosa IC, Dionísio G, Gomes-Pereira J, Paula JR, Figueiredo C, Bandarra N, Calado R, Rosa R (2016) “Gone with the wind”: fatty acid biomarkers and chemotaxonomy of stranded pleustonic hydrozoans (Velella velella and Physalia physalis). Biochem Syst Ecol 66:297–306

    Article  CAS  Google Scholar 

  • Lucas CH, Dawson MN (2014) What are jellyfish and Thaliaceans and why do they bloom? In: Pitt KA, Lucas CH (eds) Jellyfish blooms. Springer, Dordrecht, pp 9–44

    Chapter  Google Scholar 

  • Lucas CH, Graham WM, Widmer C (2012) Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Adv Mar Biol 63:133–196

    Article  PubMed  Google Scholar 

  • Ludwig F-D (1969) Die Zooxanthellan bei Cassiopea andromeda Eschscholtz 1829 (Polyp-Stadium) und ihre Bedeutung für die Strobilation. Zoologische Jahrbücher. Abt Anat Ontog Tiere 86:238–277

    Google Scholar 

  • Mackas DL, Greve W, Edwards M, Chiba S, Tadokoro K, Eloire D, Mazzochi MG, Batten S, Richardson AJ, Johnson C, Head E, Conversi A, Peluso T (2012) Changing zooplankton seasonality in a changing ocean: comparing time series of zooplankton phenology. Prog Oceanogr 97:31–62

    Article  Google Scholar 

  • Mangan J (1909) The entry of zooxanthellae into the ovum of Millepora, and some particulars concerning the medusae. J Cell Sci 53:697–710

    Google Scholar 

  • Maronna MM, Miranda TP, Peña Cantero ÁL, Barbeitos MS, Marques AC (2016) Towards a phylogenetic classification of Leptothecata (Cnidaria, Hydrozoa). Sci Rep 6:18075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marques AC, Peña Cantero AL, Vervoort W (2000) Mediterranean species of Eudendrium Ehrenberg, 1834 (Hydrozoa, Anthomedusae, Eudendriidae) with the description of a new species. J Zool Soc London 252:197–213

    Article  Google Scholar 

  • Martin LE, Dawson MN, Bell LJ, Colin PL (2006) Marine lake ecosystem dynamics illustrate ENSO variation in the tropical western Pacific. Biol Lett 2:144–147

    Article  PubMed  Google Scholar 

  • McCloskey LR, Muscatine L, Wilkerson FP (1994) Daily photosynthesis, respiration, and carbon budgets in a tropical marine jellyfish (Mastigias sp.). Mar Biol 119:13–22

    Article  Google Scholar 

  • McGill CJ, Pomoroy CM (2008) Effects of bleaching and nutrient supplementation on wet weight in the jellyfish Cassiopea xamachana (Bigelow) (Cnidaria: Scyphozoa). Mar Freshw Behav Physiol 41:179–189

    Article  Google Scholar 

  • Medel MD, Vervoort W (1995) Plumularian hydroids (Cnidaria: Hydrozoa) from the Strait of Gibraltar and nearby areas. Zool Verh 300:1–72

    Google Scholar 

  • Mellas RE, McIlroy SE, Fitt WK, Coffroth MA (2014) Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp. J Exp Mar Biol Ecol 459:38–44

    Article  Google Scholar 

  • Mergner H, Svoboda A (1977) Productivity and seasonal changes in selected reef areas in the Gulf of Aquaba (Red Sea). Helgol Meeresunters 30:383–399

    Article  Google Scholar 

  • Mies M, Güth AZ, Tenório AA, Banha TNS, Waters LG, Polito PS, Taniguchi S, Bícego MC, Sumida PYG (2018) In situ shifts of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia hispida: an approach using fatty acid trophic markers. Coral Reefs 37:677–689

    Article  Google Scholar 

  • Montgomery MK, Kremer PM (1995) Transmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata. Mar Biol 124:147–155

    Article  Google Scholar 

  • Morandini AC, Stampar SN, Maronna MM, da Silveira FL (2017) All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. J Mar Biol Assoc UK 97:321–328

    Article  Google Scholar 

  • Mortillaro JM, Pitt KA, Lee SY, Meziane T (2009) Light intensity influences the production and translocation of fatty acids by zooxanthellae in the jellyfish Cassiopea sp. J Exp Mar Biol Ecol 378:22–30

    Article  CAS  Google Scholar 

  • Moura CJ, Lessios H, Cortés J, Nizinski MS, Reed J, Santos RS, Collins AG (2018) Hundreds of genetic barcodes of the species-rich hydroid superfamily Plumularioidea (Cnidaria, Medusozoa) provide a guide toward more reliable taxonomy. Sci Rep 8:17986

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muscatine L (1974) Endosymbiosis of cnidarians and algae. In: Muscattine L, Lenhoff HM (eds) Coelenterate biology: reviews and new perspectives. Academic Press, New York, pp 359–395

    Chapter  Google Scholar 

  • Muscatine L, Marian RE (1982) Dissolved inorganic nitrogen flux in symbiotic and nonsymbiotic medusae. Limnol Oceanogr 27:910–917

    Article  CAS  Google Scholar 

  • Muscatine L, Wilkerson FP, McCloskey LR (1986) Regulation of population density of symbiotic algae in a tropical marine jellyfish (Mastigias sp.). Mar Ecol Prog Ser 32:279–290

    Article  Google Scholar 

  • Nawrocki AM, Schuchert P, Cartwright P (2010) Phylogenetics and the evolution of Capitata (Cnidaria: Hydrozoa), and the systematics of Corynidae. Zool Scr 39:290–304

    Article  Google Scholar 

  • Newkirk CR, Frazer TK, Martindale MQ (2018) Acquisition and proliferation of algal symbionts in bleached polyps of the upside-down jellyfish, Cassiopea xamachana. J Expl Mar Biol Ecol 508:44–51

    Article  Google Scholar 

  • Ohdera AH, Abrams MJ, Ames CL, Baker DM, Suescún-Bolivar LP, Collins AG, Freeman CJ, Gamero-Mora E, Goulet TL, Hofmann DK, Jaimes-Becerra A, Long PF, Marques AC, Miller LA, Mydlarz LD, Morandini AC, Newkirk CR, Putri SP, Samson JE, Stampar SN, Steinworth B, Templeman M, Thomé PE, Vlok M, Woodley CM, Wong JCY, Martindale MQ, Fitt WK, Medina M (2018) Upside-down but headed in the right direction: review of the highly versatile Cassiopea xamachana system. Front Ecol Evol 6:35

    Article  Google Scholar 

  • Ortiz-Corp’s E, Cutress CE, Cutress BM (1987) Life history of the Coronate scyphozoan Linuche unguiculata (Swartz, 1788). Caribb J Sci 23:432–443

    Google Scholar 

  • Pagliara P, Bouillon J, Boero F (2000) Photosynthetic planulae and planktonic hydroids: contrasting strategies of propagule survival. Sci Mar 64:173–178

    Article  Google Scholar 

  • Peach MB, Pitt KA (2005) Morphology of the nematocysts of the medusae of two scyphozoans, Catostylus mosaicus and Phyllorhiza punctata (Rhizostomeae): implication for capture of prey. Invertebr Biol 124:98–108

    Article  Google Scholar 

  • Pérez-Ruzafa A, Gilabert J, Gutiérrez JM, Fernández AI, Marcos C, Sabah S (2002) Evidence of a planktonic food web response to changes in nutrient input dynamics in the Mar Menor coastal lagoon, Spain. Hydrobiologia 475(476):359–369

    Article  Google Scholar 

  • Pitt KA, Koop K, Rissik D, Kingsford MJ (2004) The ecology of scyphozoan jellyfish in Lake Illawara. Wetlands (Australia) 21:115–123

    Google Scholar 

  • Pitt KA, Koop K, Rissik D (2005) Contrasting contributions to inorganic nutrient recycling by the co-occuring jellyfishes, Catostylus mosaicus and Phyllorhiza punctata (Scyphozoa, Rhizostomeae). J Exp Mar Biol Ecol 315:71–86

    Article  CAS  Google Scholar 

  • Pitt KA, Welsh DT, Condon RH (2009) Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia 616:133–149

    Article  CAS  Google Scholar 

  • Prieto L, Astorga D, Navarro G, Ruiz J (2010) Environmental control of phase transition and polyp survival of a massive-outbreaker Jellyfish. PLoS One 5:e13793

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Probert I, Siano R, Poirier C, Decelle J, Biard T, Tuji A, Suzuki N, Not F (2014) Brandtodinium gen. nov. and B. nutricula comb. nov. (Dinophyceae) a dinoflagellate commonly found in symbiosis with polycistine radiolarians. J Phycol 50:388–399

    Article  CAS  PubMed  Google Scholar 

  • Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Ann Rev Mar Sci 4:209–235

    Article  PubMed  Google Scholar 

  • Purcell JE, Clarkin E, Doyle TK (2012a) Foods of Velella velella (Cnidaria: Hydrozoa) in algal rafts and its distribution in Irish seas. Hydrobiologia 690:47–55

    Article  CAS  Google Scholar 

  • Purcell JE, Atienza D, Fuentes V, Olariaga A, Tilves U, Colahan C, Gili J-M (2012b) Temperature effects on asexual reproduction rates of scyphozoan species from the northwest Mediterranean Sea. Hydrobiologia 690:169–180

    Article  CAS  Google Scholar 

  • Purcell JE, Milisenda G, Rizzo A, Carrion SA, Zampardi S, Airoldi S, Zagami G, Guglielmo L, Boero F, Doyle TK, Piraino S (2015) Digestion and predation rates of zooplankton by the pleustonic hydrozoan Velella velella and widespread blooms in 2013 and 2014. J Plankton Res 37:1056–1067

    Article  Google Scholar 

  • Rahat M, Adar O (1980) Effect of symbiotic zooxanthellae and temperature on budding and strobilation in Cassiopea andromeda (Eschscholz). Biol Bull 159:394–401

    Article  Google Scholar 

  • Rippingale RJ, Kelly SJ (1995) Reproduction and survival of Phyllorhiza punctata (Cnidaria: Rhizostomeae) in a seasonally fluctuating salinity regime in Western Australia. Mar Freshw Res 46:1145–1151

    Article  Google Scholar 

  • Ruiz J, Prieto L, Astorga D (2012) A model for temperature control of jellyfish (Cotylorhiza tuberculata) outbreaks: a causal analysis in a Mediterranean coastal lagoon. Ecol Modell 233:59–69

    Article  Google Scholar 

  • Santhanakrishnan A, Dollinger M, Hamlet CL, Colin SP, Miller LA (2012) Flow structure and transport characteristics of feeding and exchange currents generated by upside-down Cassiopea jellyfish. J Exp Biol 215:2369–2381

    Article  PubMed  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie RA III, Hidaka M, Sakai K, Coffroth MA (2003) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenetics Evol 23:97–111

    Article  CAS  Google Scholar 

  • Schiariti A, Morandini AC, Jarms G, von Glehn Paes R, Franke S, Mianzan H (2014) Asexual reproduction strategies and blooming potential in Scyphozoa. Mar Ecol Prog Ser 510:241–253

    Article  Google Scholar 

  • Simpson GG (1953) The major features of evolution. Columbia University Press, New York

    Book  Google Scholar 

  • Soong K, Cho LC (1998) Synchronized release of medusae from three species of hydrozoan fire corals. Coral Reefs 17:145–154

    Article  Google Scholar 

  • Stoecker DK, Johnson MD, de Vargas C, Not F (2009) Acquired phototrophy in aquatic protists. Aquat Microb Ecol 57:279–310

    Article  Google Scholar 

  • Stoner EW, Layman CA, Yeager LA, Hasset HM (2011) Effects of anthropogenic disturbance on the abundance and size of epibenthic jellyfish Cassiopea spp. Mar Pollut Bull 62:1109–1114

    Article  CAS  PubMed  Google Scholar 

  • Straehler-Pohl I, Jarms G (2010) Identification key for young ephyrae: a first step for early detection of jellyfish blooms. Hydrobiologia 645:3–21

    Article  Google Scholar 

  • Straehler-Pohl I, Jarms G (2011) Morphology and life cycle of Carybdea morandinii, sp. nov. (Cnidaria), a cubozoan with zooxanthellae and peculiar polyp anatomy. Zootaxa 2755:36–56

    Article  Google Scholar 

  • Straehler-Pohl I, Toshino S (2015) Carybdea morandinii—New investigations on its life cycle reveal its true genus: Carybdea morandinii Straehler-Pohl & Jarms, 2011 becomes Alatina morandinii (Straehler-Pohl & Jarms, 2011). Plankton Benthos Res 10:167–177

    Article  Google Scholar 

  • Sugiura Y (1963) On the life-history of Rhizostome medusae I. Mastigias papua L. Agassiz Annot Zool Jpn 36:194–202

    Google Scholar 

  • Sugiura Y (1964) On the life-history of Rhizostome medusae II. Indispensability of zooxanthellae for strobilation in Mastigias papua. Embryologia 8:223–233

    Article  Google Scholar 

  • Sugiura Y (1965) On the life-history of Rhizostome medusae III. On the effects of temperature on the strobilation of Mastigias papua. Biol Bull 128:493–496

    Article  Google Scholar 

  • Sugiura Y (1969) On the life-history of Rhizostome medusae V. On the relation between zooxanthellae and the strobilation of Cephea cephea. Bull Mar Biol Stn Asamushi 8:227–233

    Google Scholar 

  • Svoboda A, Cornelius PFS (1991) The European and Mediterranean species of Aglaophenia (Cnidaria: Hydrozoa). Zool Verh 274:4–72

    Google Scholar 

  • Swift HF, Gómez Daglio L, Dawson MN (2016) Three routes to crypsis: Stasis, convergence, and parallelism in the Mastigias species complex (Scyphozoa, Rhizostomeae). Mol Phylogenetics Evol 99:103–115

    Article  CAS  Google Scholar 

  • Thornhill DJ, Daniel MW, LaJeunesse TC, Schmidt GW, Fitt WK (2006) Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. J Exp Mar Biol Ecol 338:50–56

    Article  Google Scholar 

  • Todd BD, Thornhill DJ, Fitt WK (2006) Patterns of inorganic phosphate uptake in Cassiopea xamachana: a bioindicator species. Mar Pollut Bull 52:515–521

    Article  CAS  PubMed  Google Scholar 

  • Tokioka T (1964) Occurrences of purplish individuals of Cephea cephea (Forskål) in the vicinity of Seto. Publ Seto Mar Biol Lab 12:149–156

    Article  Google Scholar 

  • Trench RK (1971) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates II. Liberation of fixed 14C by zooxanthellae in vitro. Proc R Soc London B 177:237–250

    Article  CAS  Google Scholar 

  • Underwood AH, Straehler-Pohl I, Carrette TJ, Sleeman J, Seymour JE (2018) Early life history and metamorphosis in Malo maxima Gershwin, 2005 (Carukiidae, Cubozoa, Cnidaria). Plankton Benthos Res 13:143–153

    Article  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbiosis in animals. J Exp Bot 59:1069–1080

    Article  CAS  PubMed  Google Scholar 

  • Verde EA, McCloskey LR (1998) Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: effect of jellyfish size and season. Mar Ecol Prog Ser 168:147–162

    Article  Google Scholar 

  • Verity PG, Purcell JE, Frischer ME (2011) Seasonal patterns in size and abundance of Phyllorhiza punctata: an invasive scyphomedusa in coastal Georgia (USA). Mar Biol 158:2219–2226

    Article  Google Scholar 

  • Welsh DT, Dunn RJK, Meziane T (2009) Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production. Hydrobiologia 635:351–362

    Article  CAS  Google Scholar 

  • Werner B (1973) New investigations on systematics and evolution of the class Scyphozoa and the phylum Cnidaria. Publ Seto Mar Biol Lab 20:35–61

    Article  Google Scholar 

  • West EJ, Pitt KA, Welsh DT, Koop K, Rissik D (2009) Top-down and bottom-up influences of jellyfish on primary productivity and planktonic assemblages. Limnol Oceanogr 54:2058–2071

    Article  Google Scholar 

  • Wilkerson FP, Kremer P (1992) DIN, DON and PO4 flux by medusa with algal symbionts. Mar Ecol Prog Ser 90:237–250

    Article  CAS  Google Scholar 

  • Wilkerson FP, Muller Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014

    Article  Google Scholar 

  • Wittenberg JB (1960) The source of carbon monoxide in the float of the portuguese man-of-war Physalia physalis L. J Exp Biol 37:698–705

    CAS  Google Scholar 

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  PubMed  Google Scholar 

  • Zeman SM, Corrales-Ugalde M, Brodeur RD, Sutherland KR (2018) Trophic ecology of the neustonic cnidarian Velella velella in the northern California Current during an extensive bloom year: insight from gut contents and stable isotope analysis. Mar Biol 165:120

    Article  CAS  Google Scholar 

Download references

Acknowledgements

First we would like to thank Patricia Kremer and Alan Verde who provided some unpublished data on Linuche unguiculata and Cassiopea xamachana, respectively. We would also like to thank Ferdinando Boero and André Cararra Morandini for pointing us to some hard to find literature. We thank Bella Galil, Ilka Straehler-Pohl and Sho Toshino for details about some of their work. We also thank Kylie Pitt and one anonymous reviewer for their valuable comments and suggestions. Finally, we thank Natalia Llopis Monferrer for the artwork in Fig. 3.

Funding

This work is part of the Ph.D. project of Nicolas Djeghri, funded by the University of Brest (UBO).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicolas Djeghri.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any work involving animals performed by any of the authors.

Additional information

Responsible Editor: S. Shumway.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by K. Pitt and an undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 646 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Djeghri, N., Pondaven, P., Stibor, H. et al. Review of the diversity, traits, and ecology of zooxanthellate jellyfishes. Mar Biol 166, 147 (2019). https://doi.org/10.1007/s00227-019-3581-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-019-3581-6

Navigation